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The dynamic transcriptome of waxy maize (Zea mays L. sinensis Kulesh) during seed development

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Abstract

Background

Waxy maize (Zea mays L. sinensis Kulesh) is a mutant of maize (Zea mays L.) with a mutation at Waxy1 (Wx1) gene locus. The seed of waxy maize has higher viscosity compared to regular maize. By now, we know little about the expression patterns of genes that involved in the seed development of waxy maize.

Objective

By analyzing the transcriptome data during waxy maize seed development, we attempt to dig out the genes that may influence the seed development of waxy maize.

Methods

The seeds of waxy maize inbred line SWL01 from six phases after pollination were used to do RNA-seq. Bioinformatics methods were used to analyze the expression patterns of the expressed genes, to identify the genes involved in waxy maize seed development.

Results

A total of 24,546 genes including 1611 transcription factors (TFs) were detected during waxy maize seed development. Coexpression analysis of expressed genes revealed the dynamic processes of waxy maize seed development. Particularly, 2457 genes including 177 TFs were specially expressed in waxy maize seed, some of which mainly involved in the process of seed dormancy and maturation. In addition, 2681, 5686, 4491, 4386, 3669 and 4624 genes were identified to be differential expressed genes (DEGs) at six phases compared to regular maize B73, and 113 DEGs among them may be key genes that lead the difference of seed development between waxy and regular maizes in milk stage.

Conclusion

In summary, we elucidated the expression patterns of expressed genes during waxy maize seed development globally. A series of genes that associated with seed development were identified in our research, which may provide an important resource for functional study of waxy maize seed development to help molecular assisted breeding.

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References

  • Asakura T, Tamura T, Terauchi K, Narikawa T, Yagasaki K, Ishimaru Y, Abe K (2012) Global gene expression profiles in developing soybean seeds. Plant Physiol Biochem 52:147–153

    Article  CAS  PubMed  Google Scholar 

  • Belmonte MF, Kirkbride RC, Stone SL, Pelletier JM, Bui AQ, Yeung EC, Hashimoto M, Fei J, Harada CM, Munoz MD et al (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci USA 110:E435–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennetzen JL, Hake SC (2009) Handbook of maize: its biology. Springer, New York

    Book  Google Scholar 

  • Bernardi J, Lanubile A, Li QB, Kumar D, Kladnik A, Cook SD, Ross JJ, Marocco A, Chourey PS (2012) Impaired auxin biosynthesis in the defective endosperm18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize. Plant Physiol 160:1318–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolduc N, Yilmaz A, Mejia-Guerra MK, Morohashi K, O'Connor D, Grotewold E, Hake S (2012) Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev 26:1685–1690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Strieder N, Krohn NG, Cyprys P, Sprunck S, Engelmann JC, Dresselhaus T (2017a) Zygotic genome activation occurs shortly after fertilization in maize. Plant Cell 29:2106–2125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Zeng B, Zhang M, Xie S, Wang G, Hauck A, Lai J (2014) Dynamic transcriptome landscape of maize embryo and endosperm development. Plant Physiol 166:252–264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen X, Feng F, Qi W, Xu L, Yao D, Wang Q, Song R (2017b) Dek35 encodes a PPR protein that affects cis-splicing of mitochondrial nad4 Intron 1 and seed development in maize. Mol Plant 10:427–441

    Article  CAS  PubMed  Google Scholar 

  • Cheng WH, Taliercio EW, Chourey PS (1996) The miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8:971–983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chourey PS, Li QB, Kumar D (2010) Sugar-hormone cross-talk in seed development: two redundant pathways of IAA biosynthesis are regulated differentially in the invertase-deficient miniature1 (mn1) seed mutant in maize. Mol Plant 3:1026–1036

    Article  CAS  PubMed  Google Scholar 

  • Coleman CE, Clore AM, Ranch JP, Higgins R, Lopes MA, Larkins BA (1997) Expression of a mutant alpha-zein creates the floury2 phenotype in transgenic maize. Proc Natl Acad Sci USA 94:7094–7097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coleman CE, Lopes MA, Gillikin JW, Boston RS, Larkins BA (1995) A defective signal peptide in the maize high-lysine mutant floury 2. Proc Natl Acad Sci USA 92:6828–6831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins GN (1909) A new type of Indian corn from China. US Department of Agriculture, Bureau of Plant Industry, Washington, DC

    Book  Google Scholar 

  • Collins NE, Moran ET, Stilborn HL (2003) Performance of broilers fed normal and waxy corn diets formulated with chick and rooster derived apparent metabolizable energy values for the grains. J Appl Poult Res 12:196–206

    Article  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform 11:485

    Article  Google Scholar 

  • Cui B, Liu Y, Gorovsky MA (2006) Deposition and function of histone H3 variants in Tetrahymena thermophila. Mol Cell Biol 26:7719–7730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davidson RM, Hansey CN, Gowda M, Childs KL, Lin H, Vaillancourt B, Sekhon RS, de Leon N, Kaeppler SM, Jiang N et al (2011) Utility of RNA sequencing for analysis of maize reproductive transcriptomes. Plant Genome 4:191–203

    Article  CAS  Google Scholar 

  • Deal RB, Henikoff S (2011) Histone variants and modifications in plant gene regulation. Curr Opin Plant Biol 14:116–122

    Article  CAS  PubMed  Google Scholar 

  • Domaschenz R, Kurscheid S, Nekrasov M, Han S, Tremethick DJ (2017) The histone variant H2A.Z is a master regulator of the epithelial-mesenchymal transition. Cell Rep 21:943–952

    Article  CAS  PubMed  Google Scholar 

  • Dumas C, Mogensen HL (1993) Gametes and fertilization: maize as a model system for experimental embryogenesis in flowering plants. Plant Cell 5:1337–1348

    Article  PubMed  PubMed Central  Google Scholar 

  • Dworkin-Rastl E, Kandolf H, Smith RC (1994) The maternal histone H1 variant, H1M (B4 protein), is the predominant H1 histone in Xenopus pregastrula embryos. Dev Biol 161:425–439

    Article  CAS  PubMed  Google Scholar 

  • Evans MM (2007) The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo Sac and leaf development. Plant Cell 19:46–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fedoroff N, Wessler S, Shure M (1983) Isolation of the transposable maize controlling elements Ac and Ds. Cell 35:235–242

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Xu H, Shen Y, Wang J (2013) Transcriptomic analysis of rice (Oryza sativa) endosperm using the RNA-Seq technique. Plant Mol Biol 81:363–378

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Chan CK (2016) Analysis of RNA-Seq data using TopHat and Cufflinks. Methods Mol Biol 1374:339–361

    Article  CAS  PubMed  Google Scholar 

  • Giroux MJ, Hannah LC (1994) ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Mol Gen Genet 243:400–408

    Article  CAS  PubMed  Google Scholar 

  • Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez-Marcos JF, Costa LM, Biderre-Petit C, Khbaya B, O'Sullivan DM, Wormald M, Perez P, Dickinson HG (2004) maternally expressed gene1 Is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16:1288–1301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutierrez-Marcos JF, Costa LM, Evans MM (2006) Maternal gametophytic baseless1 is required for development of the central cell and early endosperm patterning in maize (Zea mays). Genetics 174:317–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Havel L, Novak FJ (1981) In vitro pollination of maize (Zea mays L.)—proof of double fertilization. Plant Cell Rep 1:26–28

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Wang H, Huang X, Wang Q, Wang J, An D, Li J, Wang W, Wu Y (2019) Maize VKS1 regulates mitosis and cytokinesis during early endosperm development. Plant Cell 31:1238–1256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingouff M, Berger F (2010) Histone3 variants in plants. Chromosoma 119:27–33

    Article  CAS  PubMed  Google Scholar 

  • Jia Y, Lisch DR, Ohtsu K, Scanlon MJ, Nettleton D, Schnable PS (2009) Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLoS Genet 5:e1000737

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jiang D, Berger F (2017) Histone variants in plant transcriptional regulation. Biochim Biophys Acta Gene Regul Mech 1860:123–130

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, Campbell MS, Stein JC, Wei X, Chin CS et al (2017) Improved maize reference genome with single-molecule technologies. Nature 546:524–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones SI, Vodkin LO (2013) Using RNA-Seq to profile soybean seed development from fertilization to maturity. PLoS ONE 8:e59270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelliher T, Starr D, Su X, Tang G, Chen Z, Carter J, Wittich PE, Dong S, Green J, Burch E et al (2019) One-step genome editing of elite crop germplasm during haploid induction. Nat Biotechnol 37:287–292

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kramer V, Shaw JR, Senior ML, Hannah LC (2015) The sh2-R allele of the maize shrunken-2 locus was caused by a complex chromosomal rearrangement. Theor Appl Genet 128:445–452

    Article  CAS  PubMed  Google Scholar 

  • Kriz AL (1989) Characterization of embryo globulins encoded by the maize Glb genes. Biochem Genet 27:239–251

    Article  CAS  PubMed  Google Scholar 

  • Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147

    Article  CAS  PubMed  Google Scholar 

  • Lai J, Dey N, Kim CS, Bharti AK, Rudd S, Mayer KF, Larkins BA, Becraft P, Messing J (2004) Characterization of the maize endosperm transcriptome and its comparison to the rice genome. Genome Res 14:1932–1937

    Article  PubMed  PubMed Central  Google Scholar 

  • Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S et al (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci USA 107:8063–8070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leroux BM, Goodyke AJ, Schumacher KI, Abbott CP, Clore AM, Yadegari R, Larkins BA, Dannenhoffer JM (2014) Maize early endosperm growth and development: from fertilization through cell type differentiation. Am J Bot 101:1259–1274

    Article  PubMed  Google Scholar 

  • Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR et al (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067

    Article  CAS  PubMed  Google Scholar 

  • Li XJ, Zhang YF, Hou M, Sun F, Shen Y, Xiu ZH, Wang X, Chen ZL, Sun SS, Small I et al (2014) Small kernel 1 encodes a pentatricopeptide repeat protein required for mitochondrial nad7 transcript editing and seed development in maize (Zea mays) and rice (Oryza sativa). Plant J 79:797–809

    Article  CAS  PubMed  Google Scholar 

  • Liu YJ, Xiu ZH, Meeley R, Tan BC (2013) Empty pericarp5 encodes a pentatricopeptide repeat protein that is required for mitochondrial RNA editing and seed development in maize. Plant Cell 25:868–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Locatelli S, Piatti P, Motto M, Rossi V (2009) Chromatin and DNA modifications in the Opaque2-mediated regulation of gene transcription during maize endosperm development. Plant Cell 21:1410–1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu DL, Lu WP (2012) Effects of protein removal on the physicochemical properties of waxy maize flours. Starch Starke 64:874–881

    Article  CAS  Google Scholar 

  • Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260

    Article  CAS  PubMed  Google Scholar 

  • Luk E, Ranjan A, Fitzgerald PC, Mizuguchi G, Huang Y, Wei D, Wu C (2010) Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome. Cell 143:725–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 9:297–300

    Article  CAS  PubMed  Google Scholar 

  • Ni J, Ma X, Feng Y, Tian Q, Wang Y, Xu N, Tang J, Wang G (2019) Updating and interaction of polycomb repressive complex 2 components in maize (Zea mays). Planta 250:573–588

    Article  CAS  PubMed  Google Scholar 

  • Over RS, Michaels SD (2014) Open and closed: the roles of linker histones in plants and animals. Mol Plant 7:481–491

    Article  CAS  PubMed  Google Scholar 

  • Perez-Montero S, Carbonell A, Moran T, Vaquero A, Azorin F (2013) The embryonic linker histone H1 variant of Drosophila, dBigH1, regulates zygotic genome activation. Dev Cell 26:578–590

    Article  CAS  PubMed  Google Scholar 

  • Schweizer L, Yerk-Davis GL, Phillips RL, Srienc F, Jones RJ (1995) Dynamics of maize endosperm development and DNA endoreduplication. Proc Natl Acad Sci USA 92:7070–7074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scippa GS, Di Michele M, Onelli E, Patrignani G, Chiatante D, Bray EA (2004) The histone-like protein H1-S and the response of tomato leaves to water deficit. J Exp Bot 55:99–109

    Article  CAS  PubMed  Google Scholar 

  • Scippa GS, Griffiths A, Chiatante D, Bray EA (2000) The H1 histone variant of tomato, H1-S, is targeted to the nucleus and accumulates in chromatin in response to water-deficit stress. Planta 211:173–181

    Article  CAS  PubMed  Google Scholar 

  • Shannon JC, Pien FM, Cao H, Liu KC (1998) Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP–glucose into amyloplasts of maize endosperms. Plant Physiol 117:1235–1252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma R, Agarwal P, Ray S, Deveshwar P, Sharma P, Sharma N, Nijhawan A, Jain M, Singh AK, Singh VP et al (2012) Expression dynamics of metabolic and regulatory components across stages of panicle and seed development in indica rice. Funct Integr Genom 12:229–248

    Article  CAS  Google Scholar 

  • Shewry PR, Napier JA, Tatham AS (1995) Seed storage proteins: structures and biosynthesis. Plant Cell 7:945–956

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shindo Y, Amodeo AA (2019) Dynamics of free and chromatin-bound histone H3 during early embryogenesis. Curr Biol 29(359–366):e354

    Google Scholar 

  • Sprague GF, Brimhall B, Hixon RM (1943) Some effects of the waxy gene in corn on properties of the endosperm starch. J Am Soc Agron 35:817–822

    Article  Google Scholar 

  • Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45:W122–W129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trivedi I, Ranjan A, Sharma YK, Sawant S (2012) The histone H1 variant accumulates in response to water stress in the drought tolerant genotype of Gossypium herbaceum L. Protein J 31:477–486

    Article  CAS  PubMed  Google Scholar 

  • Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc Natl Acad Sci USA 94:7685–7690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Zhu L, Zhao B, Zhao Y, Xie Y, Zheng Z, Li Y, Sun J, Wang H (2019) Development of a haploid-inducer mediated genome editing system for accelerating maize breeding. Mol Plant 12:597–602

    Article  PubMed  CAS  Google Scholar 

  • Wang G, Qi W, Wu Q, Yao D, Zhang J, Zhu J, Wang G, Wang G, Tang Y, Song R (2014) Identification and characterization of Maize floury4 as a novel semidominant opaque mutant that disrupts protein body assembly. Plant Physiol 165:582–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Elling AA, Li X, Li N, Peng Z, He G, Sun H, Qi Y, Liu XS, Deng XW (2009) Genome-wide and organ-specific landscapes of epigenetic modifications and their relationships to mRNA and small RNA transcriptomes in maize. Plant Cell 21:1053–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu JH, Messing J (2009) Amplification of prolamin storage protein genes in different subfamilies of the Poaceae. Theor Appl Genet 119:1397–1412

    Article  CAS  PubMed  Google Scholar 

  • Yeung KY, Haynor DR, Ruzzo WL (2001) Validating clustering for gene expression data. Bioinformatics 17:309–318

    Article  CAS  PubMed  Google Scholar 

  • Yi F, Gu W, Chen J, Song N, Gao X, Zhang X, Zhou Y, Ma X, Song W, Zhao H et al (2019) High temporal-resolution transcriptome landscape of early maize seed development. Plant Cell 31:974–992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young TE, Gallie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol 115:737–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng M (1987) The genetic relationship of waxy maize in China. China Seed Ind 3:8–10

    Google Scholar 

  • Zhan J, Li G, Ryu CH, Ma C, Zhang S, Lloyd A, Hunter BG, Larkins BA, Drews GN, Wang X et al (2018) Opaque-2 regulates a complex gene network associated with cell differentiation and storage functions of maize endosperm. Plant Cell 30:2425–2446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhan J, Thakare D, Ma C, Lloyd A, Nixon NM, Arakaki AM, Burnett WJ, Logan KO, Wang D, Wang X et al (2015) RNA sequencing of laser-capture microdissected compartments of the maize kernel identifies regulatory modules associated with endosperm cell differentiation. Plant Cell 27:513–531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zlatanova J, Thakar A (2008) H2A.Z: view from the top. Structure 16:166–179

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by grant from The Youth Talent Development Plan of Shanghai Municipal Agricultural System of Shanghai Rural Agriculture Commission, China (Grant No. 20180107).

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HZ, WG and DY designed the experiments. WG, DY, YG, HW, TQ, PS, YH, and JW performed the experiments. WG and DY analyzed the data. WG, DY and HZ wrote the pater. Correspondence and requests for materials should be addressed to HZ (hjzh6188@163.com).

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Correspondence to Hongjian Zheng.

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Gu, W., Yu, D., Guan, Y. et al. The dynamic transcriptome of waxy maize (Zea mays L. sinensis Kulesh) during seed development. Genes Genom 42, 997–1010 (2020). https://doi.org/10.1007/s13258-020-00967-z

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